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References

  1. Boelee NC, Temmink H, Janssen M, Buisman CJN, Wijffels RH. 2014. Balancing the organic load and light supply in symbiotic microalgal–bacterial biofilm reactors treating synthetic municipal wastewater. Ecol. Eng. 64: 213-221.
    CrossRef
  2. Cai T, Park SY, Li Y. 2013. Nutrient r ecovery from wastewater streams by microalgae: status and prospects. Renew. Sust. Energ. Rev. 19: 360-369.
    CrossRef
  3. Cardozo KH, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, et al. 2007. Metabolites from algae with economical impact. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 146: 60-78.
  4. Choi O, Das A, Yu CP, Hu ZQ. 2010. Nitrifying bacterial growth inhibition in the presence of algae and cyanobacteria. Biotechnol. Bioeng. 107: 1004-1011.
    Pubmed CrossRef
  5. Daum M, Zimmer W, Papen H, Kloos K, Nawrath K, Bothe H. 1998. Physiological and molecular biological characterization of ammonia oxidation of the heterotrophic nitrifier Pseudomonas putida. Curr. Microbiol. 37: 281-288.
    Pubmed CrossRef
  6. de-Bashan LE, Moreno M, Hernandez J-P, Bashan Y. 2002. Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum brasilense. Water Res. 36: 2941-2948.
    CrossRef
  7. Gantar M, Obreht Z, Dalmacija B. 1991. Nutrient removal and algal succession during the growth of Spirulina platensis and Scenedesmus quadricauda on swine wastewater. Bioresour. Technol. 36: 167-171.
    CrossRef
  8. Godos I, González C, Becares E, García-Encina P, Muñoz R. 2009. Simultaneous nutrients and carbon removal during pretreated swine slurry degradation in a tubular biofilm photobioreactor. Appl. Microbiol. Biotechnol. 82: 187-194.
    Pubmed CrossRef
  9. González LE, Cañizares RO, Baena S. 1997. Efficiency of ammonia and phosphorus removal from a Colombian agroindustrial wastewater by the microalgae Chlorella vulgaris and Scenedesmus dimorphus. Bioresour. Technol. 60: 259-262.
    CrossRef
  10. Han H-G, Qiao J-F. 2012. Prediction of activated sludge bulking based on a self-organizing RBF neural network. J. Process Control 22: 1103-1112.
    CrossRef
  11. Harms G, Layton AC, Dionisi HM, Gregory IR, Garrett VM, Hawkins SA, et al. 2003. Real-time PCR quantification of nitrifying bacteria in a municipal wastewater treatment plant. Environ. Sci. Technol. 37: 343-351.
    Pubmed CrossRef
  12. He P, Mao B, Lü F, Shao L, Lee D, C hang J. 2013. The combined effect of bacteria and Chlorella vulgaris on the treatment of municipal wastewaters. Bioresour. Technol. 146:562-568.
    Pubmed CrossRef
  13. Hong HC, Wong MH, Mazumder A, Liang Y. 2008. Trophic state, natural organic matter content, and disinfection byproduct formation potential of six drinking water reservoirs in the Pearl River Delta, China. J. Hydrol. 359: 164-173.
    CrossRef
  14. Huang X, Li W, Zhang D, Qin W. 2013. Ammonium removal by a novel oligotrophic Acinetobacter sp. Y16 capable of heterotrophic nitrification–aerobic denitrification at low temperature. Bioresour. Technol. 146: 44-50.
    Pubmed CrossRef
  15. Jimenez J, Miller M, Bott C, Murthy S, De Clippeleir H, Wett B. 2015. High-rate activated sludge system for carbon management – Evaluation of crucial process mechanisms and design parameters. Water Res. 87: 478-482.
    Pubmed CrossRef
  16. Joo H-S, Hirai M, Shoda M. 2005. Characteristics of ammonium removal by heterotrophic nitrification-aerobic denitrification by Alcaligenes faecalis No. 4. J. Biosci. Bioeng. 100: 184-191.
    Pubmed CrossRef
  17. Karya N, Van der Steen N, Lens P. 2013. Photo-oxygenation to support nitrification in an algal–bacterial consortium treating artificial wastewater. Bioresour. Technol. 134: 244-250.
    Pubmed CrossRef
  18. Kim H-C, Choi WJ, Ryu JH, Maeng SK, Kim HS, Lee B-C, Song KG. 2014. Optimizing cultivation strategies for robust algal growth and consequent removal of inorganic nutrients in pretreated livestock effluent. Appl. Biochem. Biotechnol. 174: 1668-1682.
    Pubmed CrossRef
  19. Kim J, Lingaraju BP, Rheaume R, Lee J-Y, Siddiqui KF. 2010. Removal of ammonia from wastewater effluent by Chlorella vulgaris. Tsinghua Sci. Technol. 15: 391-396.
    CrossRef
  20. Kim J, Liu Z, Lee J-Y, Lu T. 2013. Removal of nitrogen and phosphorus from municipal wastewater effluent using Chlorella vulgaris and its growth kinetics. Desalination Water Treat. 51: 7800-7806.
    CrossRef
  21. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, et al. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62: 716-721.
    Pubmed CrossRef
  22. Kouzuma A, Watanabe K. 2015. Exploring the potential of algae/bacteria interactions. Curr. Opin. Biotechnol. 33: 125-129.
    Pubmed CrossRef
  23. Leflaive J, Ten-Hage L. 2007. Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshwater Biol. 52: 199-214.
    CrossRef
  24. Luo J, W ang Y, Tang S, L iang J, Lin W, Luo L. 2013. Isolation and identification of algicidal compound from Streptomyces and algicidal mechanism to Microcystis aeruginosa. PLoS One 8: e76444.
    Pubmed PMC CrossRef
  25. Ma HF, Zhuang LN, Li F. 2012. Comparison study on growth, removal of nitrogen and phosphorus, and nutritional property of two species of microalgae. Appl. Mech. Mater. 209: 1923-1928.
    CrossRef
  26. Mamais D, Noutsopoulos C, Dimopoulou A, Stasinakis A, Lekkas TD. 2015. Wastewater treatment process impact on energy savings and greenhouse gas emissions. Water Sci. Technol. 71: 303-308.
    Pubmed CrossRef
  27. Manage PM, Kawabata Z, Nakano S. 2000. Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat. Microb. Ecol. 22: 111-117.
    CrossRef
  28. Markou G, Nerantzis E. 2013. Microalgae for high-value compounds and biofuels production: a review with focus on cultivation under stress conditions. Biotechnol. Adv. 31: 1532-1542.
    Pubmed CrossRef
  29. Mook W, Chakrabarti M, Aroua M, Khan G, Ali B, Islam M, Hassan MA. 2012. Removal of total ammonia nitrogen (TAN), nitrate and total organic carbon (TOC) from aquaculture wastewater using electrochemical technology: a review. Desalination 285: 1-13.
    CrossRef
  30. Muñoz R, Guieysse B. 2006. Algal–bacterial processes for the treatment of hazardous contaminants: a review. Water Res. 40: 2799-2815.
    Pubmed CrossRef
  31. Muñoz R, Köllner C, Guieysse B, Mattiasson B. 2003. Salicylate biodegradation by various algal-bacterial consortia under photosynthetic oxygenation. Biotechnol. Lett. 25: 1905-1911.
    CrossRef
  32. Sartory D, Grobbelaar J. 1984. Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114: 177-187.
    CrossRef
  33. Silva-Benavides AM, Torzillo G. 2012. Nitrogen and phosphorus removal through laboratory batch cultures of microalga Chlorella vulgaris and cyanobacterium Planktothrix isothrix grown as monoalgal and as co-cultures. J. Appl. Phycol. 24: 267-276.
    CrossRef
  34. Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkateswarlu K, Naidu R. 2011. Consortia of cyanobacteria/microalgae and bacteria: biotechnological potential. Biotechnol. Adv. 29: 896-907.
    Pubmed CrossRef
  35. Suzuki MT, Giovannoni SJ. 1996. Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl. Environ. Microbiol. 62: 625-630.
    Pubmed PMC
  36. Tang HL, Chen H. 2015. Nitrification at full-scale municipal wastewater treatment plants: evaluation of inhibition and bioaugmentation of nitrifiers. Bioresour. Technol. 190: 76-81.
    Pubmed CrossRef
  37. Theodoridis G, Gika HG, Wilson ID. 2008. LC-MS-based methodology for global metabolite profiling in metabonomics/metabolomics. Trends Analyt. Chem. 27: 251-260.
    CrossRef
  38. Zhang E , Wang B , Wang Q , Zhang S, Zhao B. 2008. Ammonia–nitrogen and orthophosphate removal by immobilized Scenedesmus sp. isolated from municipal wastewater for potential use in tertiary treatment. Bioresour. Technol. 99:3787-3793.
    Pubmed CrossRef
  39. Zhao L, Chen L, Yin P. 2014. Algicidal metabolites produced by Bacillus sp. strain B1 against Phaeocystis globosa. J. Ind. Microbiol. Biotechnol. 41: 593-599.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(5): 900-908

Published online May 28, 2016 https://doi.org/10.4014/jmb.1512.12067

Copyright © The Korean Society for Microbiology and Biotechnology.

Effect of Algal Inoculation on COD and Nitrogen Removal, and Indigenous Bacterial Dynamics in Municipal Wastewater

Jangho Lee 1, Jaejin Lee 2, 3, Sudheer Kumar Shukla 1, Joonhong Park 1 and Tae Kwon Lee 4*

1School of Civil and Environmental Engineering, Yonsei University, Seoul 03722, Republic of Korea, 2Division of Polar Life Sciences, Korea Polar Research Institute, Incheon 21990, Republic of Korea, 3Center for Environmental Biotechnology, University of Tennessee, Knoxville, TN 37996-0865, USA, 4Department of Environmental Engineering, Yonsei University, Wonju 26493, Republic of Korea

Received: December 28, 2015; Accepted: February 26, 2016

Abstract

The effects of algal inoculation on chemical oxygen demand (COD) and total nitrogen (TN)
removal, and indigenous bacterial dynamics were investigated in municipal wastewater.
Experiments were conducted with municipal wastewater inoculated with either Chlorella
vulgaris AG10032, Selenastrum gracile UTEX 325, or Scenedesmus quadricauda AG 10308.
C. vulgaris and S. gracile as fast growing algae in municipal wastewater, performed high COD
and TN removal in contrast to Sc. quadricauda. The indigenous bacterial dynamics revealed by
16S rRNA gene amplification showed different bacterial shifts in response to different algal
inoculations. The dominant bacterial genera of either algal case were characterized as
heterotrophic nitrifying bacteria. Our results suggest that selection of indigenous bacteria that
symbiotically interact with algal species is important for better performance of wastewater
treatment.

Keywords: municipal wastewater, algal inoculation, bacterial dynamics, COD and nitrogen removal, algal-bacterial consortia

References

  1. Boelee NC, Temmink H, Janssen M, Buisman CJN, Wijffels RH. 2014. Balancing the organic load and light supply in symbiotic microalgal–bacterial biofilm reactors treating synthetic municipal wastewater. Ecol. Eng. 64: 213-221.
    CrossRef
  2. Cai T, Park SY, Li Y. 2013. Nutrient r ecovery from wastewater streams by microalgae: status and prospects. Renew. Sust. Energ. Rev. 19: 360-369.
    CrossRef
  3. Cardozo KH, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, et al. 2007. Metabolites from algae with economical impact. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 146: 60-78.
  4. Choi O, Das A, Yu CP, Hu ZQ. 2010. Nitrifying bacterial growth inhibition in the presence of algae and cyanobacteria. Biotechnol. Bioeng. 107: 1004-1011.
    Pubmed CrossRef
  5. Daum M, Zimmer W, Papen H, Kloos K, Nawrath K, Bothe H. 1998. Physiological and molecular biological characterization of ammonia oxidation of the heterotrophic nitrifier Pseudomonas putida. Curr. Microbiol. 37: 281-288.
    Pubmed CrossRef
  6. de-Bashan LE, Moreno M, Hernandez J-P, Bashan Y. 2002. Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum brasilense. Water Res. 36: 2941-2948.
    CrossRef
  7. Gantar M, Obreht Z, Dalmacija B. 1991. Nutrient removal and algal succession during the growth of Spirulina platensis and Scenedesmus quadricauda on swine wastewater. Bioresour. Technol. 36: 167-171.
    CrossRef
  8. Godos I, González C, Becares E, García-Encina P, Muñoz R. 2009. Simultaneous nutrients and carbon removal during pretreated swine slurry degradation in a tubular biofilm photobioreactor. Appl. Microbiol. Biotechnol. 82: 187-194.
    Pubmed CrossRef
  9. González LE, Cañizares RO, Baena S. 1997. Efficiency of ammonia and phosphorus removal from a Colombian agroindustrial wastewater by the microalgae Chlorella vulgaris and Scenedesmus dimorphus. Bioresour. Technol. 60: 259-262.
    CrossRef
  10. Han H-G, Qiao J-F. 2012. Prediction of activated sludge bulking based on a self-organizing RBF neural network. J. Process Control 22: 1103-1112.
    CrossRef
  11. Harms G, Layton AC, Dionisi HM, Gregory IR, Garrett VM, Hawkins SA, et al. 2003. Real-time PCR quantification of nitrifying bacteria in a municipal wastewater treatment plant. Environ. Sci. Technol. 37: 343-351.
    Pubmed CrossRef
  12. He P, Mao B, Lü F, Shao L, Lee D, C hang J. 2013. The combined effect of bacteria and Chlorella vulgaris on the treatment of municipal wastewaters. Bioresour. Technol. 146:562-568.
    Pubmed CrossRef
  13. Hong HC, Wong MH, Mazumder A, Liang Y. 2008. Trophic state, natural organic matter content, and disinfection byproduct formation potential of six drinking water reservoirs in the Pearl River Delta, China. J. Hydrol. 359: 164-173.
    CrossRef
  14. Huang X, Li W, Zhang D, Qin W. 2013. Ammonium removal by a novel oligotrophic Acinetobacter sp. Y16 capable of heterotrophic nitrification–aerobic denitrification at low temperature. Bioresour. Technol. 146: 44-50.
    Pubmed CrossRef
  15. Jimenez J, Miller M, Bott C, Murthy S, De Clippeleir H, Wett B. 2015. High-rate activated sludge system for carbon management – Evaluation of crucial process mechanisms and design parameters. Water Res. 87: 478-482.
    Pubmed CrossRef
  16. Joo H-S, Hirai M, Shoda M. 2005. Characteristics of ammonium removal by heterotrophic nitrification-aerobic denitrification by Alcaligenes faecalis No. 4. J. Biosci. Bioeng. 100: 184-191.
    Pubmed CrossRef
  17. Karya N, Van der Steen N, Lens P. 2013. Photo-oxygenation to support nitrification in an algal–bacterial consortium treating artificial wastewater. Bioresour. Technol. 134: 244-250.
    Pubmed CrossRef
  18. Kim H-C, Choi WJ, Ryu JH, Maeng SK, Kim HS, Lee B-C, Song KG. 2014. Optimizing cultivation strategies for robust algal growth and consequent removal of inorganic nutrients in pretreated livestock effluent. Appl. Biochem. Biotechnol. 174: 1668-1682.
    Pubmed CrossRef
  19. Kim J, Lingaraju BP, Rheaume R, Lee J-Y, Siddiqui KF. 2010. Removal of ammonia from wastewater effluent by Chlorella vulgaris. Tsinghua Sci. Technol. 15: 391-396.
    CrossRef
  20. Kim J, Liu Z, Lee J-Y, Lu T. 2013. Removal of nitrogen and phosphorus from municipal wastewater effluent using Chlorella vulgaris and its growth kinetics. Desalination Water Treat. 51: 7800-7806.
    CrossRef
  21. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, et al. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62: 716-721.
    Pubmed CrossRef
  22. Kouzuma A, Watanabe K. 2015. Exploring the potential of algae/bacteria interactions. Curr. Opin. Biotechnol. 33: 125-129.
    Pubmed CrossRef
  23. Leflaive J, Ten-Hage L. 2007. Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshwater Biol. 52: 199-214.
    CrossRef
  24. Luo J, W ang Y, Tang S, L iang J, Lin W, Luo L. 2013. Isolation and identification of algicidal compound from Streptomyces and algicidal mechanism to Microcystis aeruginosa. PLoS One 8: e76444.
    Pubmed KoreaMed CrossRef
  25. Ma HF, Zhuang LN, Li F. 2012. Comparison study on growth, removal of nitrogen and phosphorus, and nutritional property of two species of microalgae. Appl. Mech. Mater. 209: 1923-1928.
    CrossRef
  26. Mamais D, Noutsopoulos C, Dimopoulou A, Stasinakis A, Lekkas TD. 2015. Wastewater treatment process impact on energy savings and greenhouse gas emissions. Water Sci. Technol. 71: 303-308.
    Pubmed CrossRef
  27. Manage PM, Kawabata Z, Nakano S. 2000. Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat. Microb. Ecol. 22: 111-117.
    CrossRef
  28. Markou G, Nerantzis E. 2013. Microalgae for high-value compounds and biofuels production: a review with focus on cultivation under stress conditions. Biotechnol. Adv. 31: 1532-1542.
    Pubmed CrossRef
  29. Mook W, Chakrabarti M, Aroua M, Khan G, Ali B, Islam M, Hassan MA. 2012. Removal of total ammonia nitrogen (TAN), nitrate and total organic carbon (TOC) from aquaculture wastewater using electrochemical technology: a review. Desalination 285: 1-13.
    CrossRef
  30. Muñoz R, Guieysse B. 2006. Algal–bacterial processes for the treatment of hazardous contaminants: a review. Water Res. 40: 2799-2815.
    Pubmed CrossRef
  31. Muñoz R, Köllner C, Guieysse B, Mattiasson B. 2003. Salicylate biodegradation by various algal-bacterial consortia under photosynthetic oxygenation. Biotechnol. Lett. 25: 1905-1911.
    CrossRef
  32. Sartory D, Grobbelaar J. 1984. Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114: 177-187.
    CrossRef
  33. Silva-Benavides AM, Torzillo G. 2012. Nitrogen and phosphorus removal through laboratory batch cultures of microalga Chlorella vulgaris and cyanobacterium Planktothrix isothrix grown as monoalgal and as co-cultures. J. Appl. Phycol. 24: 267-276.
    CrossRef
  34. Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkateswarlu K, Naidu R. 2011. Consortia of cyanobacteria/microalgae and bacteria: biotechnological potential. Biotechnol. Adv. 29: 896-907.
    Pubmed CrossRef
  35. Suzuki MT, Giovannoni SJ. 1996. Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl. Environ. Microbiol. 62: 625-630.
    Pubmed KoreaMed
  36. Tang HL, Chen H. 2015. Nitrification at full-scale municipal wastewater treatment plants: evaluation of inhibition and bioaugmentation of nitrifiers. Bioresour. Technol. 190: 76-81.
    Pubmed CrossRef
  37. Theodoridis G, Gika HG, Wilson ID. 2008. LC-MS-based methodology for global metabolite profiling in metabonomics/metabolomics. Trends Analyt. Chem. 27: 251-260.
    CrossRef
  38. Zhang E , Wang B , Wang Q , Zhang S, Zhao B. 2008. Ammonia–nitrogen and orthophosphate removal by immobilized Scenedesmus sp. isolated from municipal wastewater for potential use in tertiary treatment. Bioresour. Technol. 99:3787-3793.
    Pubmed CrossRef
  39. Zhao L, Chen L, Yin P. 2014. Algicidal metabolites produced by Bacillus sp. strain B1 against Phaeocystis globosa. J. Ind. Microbiol. Biotechnol. 41: 593-599.
    Pubmed CrossRef